Preoperative simulation using 3D-CT angiography in splenic flexure colon cancer: a retrospective observational study

doi:10.21203/rs.3.rs-1859958/v1

Purpose: This study aimed to evaluate the extent of lymph node dissection (LND) determined using preoperative Three-dimensional computed tomography angiography (3D-CTA), in the management of splenic flexure colon cancer (SFC).

Methods: In this retrospective observational study, sixty patients who underwent preoperative 3D-CTA and laparoscopic complete mesocolic excision for SFC between September 2012 and December 2021 were identified at a tertiary care center in Japan. Preoperative 3D-CTA was used to confirm the feeding arteries, following which the extent of LND was determined. Left hemicolectomy (LHC) was performed in cases requiring LND in the domains of the middle colic artery and left colic artery. In other cases, a partial colectomy (PC) that was defined as a segmental resection of the splenic flexure with LND in the domains of the feeding arterie(s) was performed. Surgical and oncological outcomes were compared between PC and LHC.

Results: Preoperative 3D-CTA enabled the evaluation of the feeding artery in all patients. PC was performed in 51 patients (85.0%). Patients who underwent PC had a shorter operating time (P=0.04) and lesser blood loss (P=0.02). There was no difference in complications between the two groups. The number of harvested lymph nodes was lower in the PC group (P=0.008); however, the number of metastatic lymph nodes was comparable. There was no significant difference in the 3-year overall survival, as well as the 3-year disease free survival.

Conclusions: Preoperative simulation using 3D-CTA has the potential to be useful in the identification of feeding arteries and determination of optimal extent of LND.

Trial registration: The trial was registered with the UMIN Clinical Trials Registry, number UMIN000047600.

Colorectal cancer

Splenic flexure colon cancer

Laparoscopic surgery

Accessory middle colic artery

Vascular anatomy

Splenic flexure

Colorectal cancer is the third most common cancer worldwide [1]. Among these, splenic flexure colon cancer (SFC) is a relatively rare condition, as it represents approximately 2 to 8% of all colon cancers [2–4]. SFC is defined as colon cancer located between the distal third of the transverse colon and the first third of the descending colon [2]. It is associated with a high risk of obstruction and poor prognosis [5–6]. Despite improvement in surgical management, surgery for SFC is yet to be standardized because lymphatic drainage at the site of surgery is variable and thus the optimal extent of lymph node dissection (LND) remains arbitrary [7–9]. Moreover, anatomical vascular variations at the splenic flexure make the surgical procedure even more complex.

Complete mesocolic excision (CME) with central vascular ligation (CVL) has been standardized as a radical surgery in colon cancer [10]. Therefore, it is important to discern the vessels that provide blood to and drain lymph from the tumor. Blood supply to the splenic flexure is derived from either the left branch of the middle colic artery (lt-MCA) that branches from the superior mesenteric artery (SMA), or the left colic artery (LCA) that branches from the inferior mesenteric artery (IMA). In addition, the accessory middle colic artery (AcMCA) drives blood supply to the splenic flexure whenever it is present [11]. It is considered that SFC has drainage roots from the lt-MCA, LCA, and AcMCA depending on the case. To perform LND at all the above areas, left hemicolectomy (LHC), with lt-MCA and LCA ligation, is considered a reasonable procedure in SFC. However, the identification of the feeding artery and optimal area(s) of LND is essential to performing CME with CVL in patients with SFC. We hypothesized that individualized LND could be performed by central ligating the feeding arteries which is identified in each patient and performing CME.

Three-dimensional computed tomography angiography (3D-CTA) has gained widespread acceptance for the preoperative evaluation of blood supply, and its accuracy and validity in various settings have been documented [12, 13]. Therefore, 3D-CTA enables preoperative identification of the feeding arteries and optimal area(s) of LND in SFC. This study aimed to evaluate the extent of LND determined by preoperative 3D-CTA in SFC.

Patients

Patients who underwent laparoscopic CME with CVL for SFC between September 2012 and December 2021were identified at Fujisawa City Hospital by the Department of Surgery. In this study, SFC was defined as a colonic adenocarcinoma with its center located between the distal third of the transverse colon and proximal third of the descending colon. Excluded from the study were patients who underwent emergency surgery, could not undergo preoperative 3D-CTA due to renal dysfunction or iodine allergy, or was missing data that was required for analysis. Institutional approval for this study was obtained from the Ethical Advisory Committee of Fujisawa City Hospital on 19/04/2022 before initiating the study (F2022003) and this study was registered in the UMIN Clinical Trials Registry as UMIN000047600 on 27/04/2022.

Preoperative simulation by 3D-CTA

Tumor localization was performed via colonoscopy and marked using an Indian ink tattoo and mucosal clip. This was followed by contrast-enhanced computed tomography (CT) examination during the arterial, portal venous, and delayed phases using a bolus tracking system. In addition, CT colonography (CTC) or barium enema examination was performed to visualize the tumor location. All CT images were analyzed and reconstructed using 3D-CTA with CTC. We preoperatively identified the feeding arteries and determined the extent of LND using 3D-CTA (Fig. 1). Feeding arteries were defined as arteries flowing within 10cm of the tumor edge because lymphatic spread of colon cancer was first located in the pericolic lymph nodes, but no more than 10 cm from the primary, and then into the lymph nodes along these arteries [10, 14]. LHC was selected as the treatment of choice if the lt-MCA, LCA, and AcMCA (when present) were the feeding arteries. In all other cases, a partial colectomy (PC) was performed. In this study, PC was defined as a segmental resection of the splenic flexure with ligation at the origin of the feeding arterie(s). In addition, vascular anatomy was confirmed, including the MCA root, presence of the AcMCA, distance between the IMA root and the LCA bifurcation, inferior mesenteric vein (IMV) inflow pattern (Fig. 2), and presence of the gastrocolic trunk (GCT).

Surgical procedure

CME with CVL was performed laparoscopically in all cases. The surgical procedure was performed using five ports: a 12 mm port in the umbilical region and 5 mm ports in the upper right, upper left, lower right, and lower left quadrants. In cases where the lt-MCA was included as a feeding artery, it was ligated at the root, and lymph nodes around the MCA were dissected. Similarly, in cases where the LCA was included as a feeding artery, it was ligated at the root and lymph nodes around the IMA root were dissected. In cases where AcMCA was present, it was exposed and ligated centrally at the dorsal pancreas. The IMV was ligated at the splenic vein (SPV) or the superior mesenteric vein (SMV) inflow site for advanced cancer (Fig. 3), or at the inferior border of the pancreas for early-stage cancer. The colon was mobilized as per the standard procedure followed in CME and removed via a 5–6 cm umbilical incision. The colon and mesocolon were dissected approximately 10 cm proximal and distal to the tumor, and the specimen was extracted. A functional end-to-end anastomosis was then performed.

Study design

In this retrospective study, patient demographic, clinicopathological data, and surgical outcomes were recorded. (Date included age, sex, body mass index (BMI), American Society of Anesthesiologists (ASA) score, surgical procedure, operative time, blood loss, Union for International Cancer Control (UICC) stage, number of harvested lymph nodes, number of metastatic lymph nodes, length of postoperative hospital stays, postoperative complications occurrence, and postoperative adjuvant chemotherapy). All patients underwent general follow-up examinations and measurements of serum CEA levels every three or six months as well as chest and abdominal CT scans every six months, and colonoscopies every year for five years post-surgery. Recurrence was confirmed histologically and/or radiologically. Overall survival (OS) was defined as the time from surgery to the date of death, while disease-free survival (DFS) was defined as the time from surgery to the date of diagnosis of local recurrence, distant metastasis, or death. Patient demographics, clinicopathological data, and OS were compared between patients who underwent PC and LHC. DFS was compared between the two groups excluding patients with pathological stage IV UICC.

Statistical Analysis

Continuous variables were presented as median along with the interquartile range (IQR). Categorical variables were presented as frequency (%). Categorical variables were compared using the chi-square test or Fisher’s exact test, and the Mann-Whitney U test, where appropriate. Statistical significance was set at α = 0.05. OS and DFS were calculated by plotting Kaplan-Meier survival curves, and differences were evaluated using the log-rank test. All analyses were performed using SPSS version 27 (IBM Corp. Armonk, NY, USA).

Patient demographics, clinicopathological dates, and surgical outcomes

Sixty patients met the inclusion criteria and were included in the final cohort. Patient demographics, clinicopathological data, and surgical outcomes are shown in Table 1. The median age was 70 (IQR 64.75-74) years, and most patients were men (n = 37, 61.7%). The median BMI was 22.2 (IQR 20.1–25.0). Most patients underwent PC (n = 51, 85%). The median operating time was 260.5 (IQR 220.25–304) min, and the median blood loss was 20 (IQR 5–50) ml. No cases were converted to laparotomy. The median number of harvested lymph nodes was 18 (IQR 11–28). Most patients had UICC pathological stage II (n = 23, 38.3%) tumors, followed by UICC pathological stage I (n = 15, 25.0%), and stage III (n = 15, 25.0%) tumors. The median length of postoperative hospital stay was 8 (IQR 7-9.25) days, and complications classified as Clavien-Dindo III and IV were observed in 10.0% of patients (n = 6) (Table 2). Roughly three-fifths of patients with pathological stage II and III (n = 22, 57.9%) were treated with postoperative adjuvant chemotherapy. Postoperative recurrence was observed in six patients, but no lymph node recurrence was observed (Table 3).

Preoperative simulation via 3D-CTA

Preoperative 3D-CTA facilitated evaluation of the feeding artery and vascular anatomy in all patients. Three patients (5%) in whom lt-MCA, AcMCA, and LCA fed the tumor and six patients (10%) in whom the lt-MCA and LCA fed the tumor underwent LHC. All other underwent PC (51 patients, 85.0%). The tumor was fed by the lt-MCA and AcMCA in five patients (8.3%), and by the AcMCA and LCA in nine patients (15%). The lt-MCA was the lone feeding artery in 10 patients (16.7%), the AcMCA was the lone feeding artery in 14 patients (23.3%), and the LCA was the lone feeding artery in 13 patients (21.6%) (Table 4 and Fig. 4). The AcMCA was present and identified in 31patients (51.7%). In 36 patients (60%), the IMV flowed into the SPV via the inferior edge of the pancreas. The IMV flowed into the SMV in 17 patients (28.3%), and into the junction of the SPV and portal vein (PV) in seven patients (11.7%).

Comparison of Outcomes in Patients with PC versus LHC

Patient age, sex, BMI, and ASA scores were comparable. Patients who underwent PC had a shorter operating time (248min [IQR 211-297.5] vs. 295min [IQR 234–420], P = 0.04) and less blood loss (15ml [IQR 5–50] vs. 50ml [IQR 30–150], P = 0.02). In patients who underwent PC, the number of harvested lymph nodes was lower (15 [IQR 11-25.5] vs. 36 [IQR 21–38], P = 0.008), but the number of metastatic lymph nodes was comparable. The UICC pathological stage, length of postoperative hospital stays, and postoperative complications classified as Clavien-Dindo III and IV were comparable. No difference in postoperative adjuvant chemotherapy was observed (Table 5).

During a median follow-up period of 46.3months (IQR 24.3–61.4), there was no significant difference in the 3-year OS (97.6% vs. 88.9%, P = 0.24), or in the 3-year DFS (91.4% vs. 87.5%, P = 0.75) (Fig. 5).

From an embryological point of view, the splenic flexure is an anatomical junction at the end of the midgut and the beginning of the hindgut. Therefore, it is supplied by either the MCA, branching from SMA, or the LCA, branching from the IMA. In addition, the AcMCA can aberrantly originate from the SMA at the inferior border of the pancreas and supply the splenic flexure [11]. For these reasons, the optimal extent of LND is uncertain. Visualizing the relationship between vascular anatomy and tumor location helps to better plan CME with CVL, considering case-to-case variations.

To remove the lymph nodes around the MCA, AcMCA, and LCA areas, LHC ligating the lt-MCA, LCA, and AcMCA, if present, is a reasonable operative procedure for SFC. Certain studies have reported that LHC is preferred in SFC [15, 16]. In addition, other literature recommends extended right hemicolectomy (ERHC) or subtotal colectomy in SFC [17]. However, there is no consensus in the literature regarding the choice of operative procedure at this site [18]. Recent studies using indocyanine green (ICG) fluorescence imaging found no case of lymph flow in both the lt-MCA and LCA areas. This finding suggests that it is not necessary to ligate both the lt-MCA and LCA in SFC [18, 19]. In colon cancer, pericolic lymph nodes are present within 10 cm of the tumor, followed by the nodes along the next arterial arcade, centrally towards the SMA or IMA [14, 20–23]. Hohenberg et al. suggested that it is important to ligate feeding arteries that flow within 10 cm of the tumor [10]. Therefore, performing LHC or ERHC in all patients with SFC should be considered excessive treatment, and the LND of the area determined by the feeding arteries should be adequate. In this study, we performed individualized CME with CVL using 3D-CTA to identify the feeding arteries.

In the comparison of outcomes in patients with PC versus those with LHC, PC had better surgical outcomes with respect to operating time and blood loss. In LHC, more vessels needed to be ligated and wider mesocolons needed to be mobilized; therefore, short-term outcomes were likely to be poor. Regarding the oncological quality of resection, it is recommended to harvest at least 12 lymph nodes [24]. In this study, the median number of harvested lymph nodes was 15 in patients with PC. In contrast, more lymph nodes were harvested in LHC. However, the number of metastatic lymph nodes was comparable between the two groups, and no cases recurred at the lymph node during follow up. Therefore, the LND performed by us in patients who underwent PC, was optimal. There was also no significant difference in long-term outcomes. These findings all suggested that individualized LND in SFC using 3D-CTA is a valid surgical option.

In addition to the existence of the AcMCA, there are many other variations in the branches of the SMA and IMA, such as the type of lt-MCA branching directly from the SMA, the long common MCA branch, the long common IMA branch, and the sigmoid artery branching from the LCA. Three drainage patterns of the IMV exist as well. The IMV drains into the SMV, SPV, or confluence of the SPV and the SMV [25–27]. These anatomical variations in vasculature complicate surgery in SFC. Therefore, a clear preoperative understanding of the vascular anatomy of the SMA, IMA, SMV, and IMV helps to avoid intraoperative injury and subsequent postoperative complications. 3D-CTA allows for excellent visualization of the mesenteric vessels [27]. During dissection of the lymph nodes at the MCA areas, it is very important to identify the GCT, the root of the MCA, and the lt-MCA branch. Preoperative simulation using 3D-CTA helps to understand the relationship between the GCT and MCA root as well as the distance of the lt-MCA branch from the MCA origin. Similarly, a preoperative understanding of the distance of the LCA branch from the IMA origin, makes it easier to identify the LCA origin intraoperatively. In a previous study, lymph flow pattern around the IMV was reported [18]. Considering the standard procedure and principle of CME with CVL, the IMV should be ligated at the confluence of the SPV and SMV. Recognition of the drainage patterns of the IMV by 3D-CTA may help identify the ligation site of the IMV intraoperatively.

This study had certain limitations. Firstly, the small sample size, retrospective nature of the study, and the single-center setting may limit the generalization of results. In particular, the number of patients who underwent LHC was small. Additionally, the follow-up period was relatively short. Further studies with a larger population and long-term follow-up are required to confirm our findings. Secondly, not all hospitals are equipped to perform 3D-CTA. In addition, a multidisciplinary approach including radiology technicians is needed, because it is necessary to reconstruct 3D-CTA images from the surgeon’s point of view. Thirdly, a previous study using ICG reported lymphatic flow from the splenic flexure along the IMV [18]. In addition to the IMV, veins flowing directly from the splenic flexure to the SPV have also been reported [28]. In this study, the extent of LND was determined by arterial domains, and the IMV was dissected at the inflow area in the case of advanced cancer, or at the inferior border of the pancreas in early-stage cancer. Consideration of the lymphatic flow associated with veins may allow for even more personalized LND. Furthermore, a certain number of patients cannot undergo contrast-enhanced CT due to renal dysfunction or allergies. In these cases, it may be difficult to identify nutrient vessels and determine the optimal area of LND.

Preoperative simulation using 3D-CTA has the potential to be a useful tool in the identification of feeding vessels, and for the determination of the optimal area of LND, with respect to surgical and oncological outcomes. In addition, 3D-CTA was considered useful for the planning of laparoscopic CME with CVL, by aiding in the evaluation of vascular anatomy preoperatively.

3D-CTA Three-dimensional computed tomography angiography

AcMCA accessory middle colic artery

ASA American Society of Anesthesiologists

BMI body mass index

CT computed tomography

CTC computed tomography colonography

CME complete mesocolic excision

CVL central vascular ligation

DFS disease-free survival

ERHC extended right hemicolectomy

GCT gastrocolic trunk

ICG indocyanine green

IMA inferior mesenteric artery

IMV inferior mesenteric vein

IQR interquartile range

LCA left colic artery

LHC left hemicolectomy

lt-MCA left branch of the middle colic artery

LND lymph node dissection

OS overall survival

PC partial colectomy

PV portal vein

SFC splenic flexure colon cancer

SMA superior mesenteric artery

SMV superior mesenteric vein

SPV splenic vein

UICC Union for International Cancer Control

Ethics approval and consent to participate: This study was conducted according to the principles of Declaration of Helsinki. Institutional approval for this study was obtained from the Ethical Advisory Committee of Fujisawa City Hospital before initiating the study (F2022003) and this study was registered in the UMIN Clinical Trials Registry as UMIN000047600. Informed consent was exempted by the Ethical Advisory Committee of Fujisawa City Hospital due to the retrospective nature of the study.

Consent for publication: Not applicable

Availability of data and materials: The approval to access the collected data used in this current study is limited by Fujisawa City Hospital, and it is not allowed to distribute or make patient data directly available to other parties. The datasets generated and/or analyzed during the current study are not publicly available due to limit by Fujisawa City Hospital and do not include allowance to forward or share data with other researchers but are available from Shigeru Yamagishi on reasonable request.

Competing interests: The authors declare that they have no competing interests

Conflict of Interest: The authors declare no conflicts of interest for this work.

Funding: No funding was received for conducting this study.

Author contributions: SY contributed to the study design. All of the authors contributed to the data collection, data analysis, and interpretation. SY and JK contributed to the statistical analyses. All of the authors contributed to the writing or review of the report and approved the final version.

Acknowledgments: We would like to thank Editage (www.editage.com) for English language editing.

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Table 1: Patient demographics, clinicopathological data, and surgical outcomes

Variable		n=60
Age (years)^a		70 (64.75-74)
Male		37 (61.7%)
BMI (kg/m²)^a		22.2 (20.1-25.0)
ASA score
	1	4 (6.7%)
	2	54 (90.0%)
	3	2 (3.3%)
Operating time (min)^a		260.5 (220.25-304)
Blood loss (ml)^a		20 (5-50)
Conversion to laparotomy		0 (0.0%)
UICC pathological Stage
	0	1 (1.7%)
	1	15 (25.0%)
	2	23 (38.3%)
	3	15 (25.0%)
	4	6 (10.0%)
Number of harvested lymph nodes^a		18 (11-28)
Number of metastatic lymph nodes^a		0 (0-1)
Length of postoperative hospital stay^a		8 (7-9.25)
Postoperative complication occurrence		6 (10%)

^aMedian (IQR)

BMI, body mass index; ASA-PS, American Society of Anesthesiologists; UICC, Union for International Cancer Control

Table 2: Complications classified as Clavien-Dindo III and IV

			surgical procedure
		n (%)	PC, n=51	LHC, n=9
Any complications		6 (10.0%)	5 (9.8%)	1 (11.1%)
	Intra-abdominal abscess	2 (3.3%)	2 (3.9%)	0 (0.0%)
	Bowel obstruction of treitz ligament	1 (1.7%)	1 (2.0%)	0 (0.0%)
	Intra-abdominal hemorrhage	1 (1.7%)	1 (2.0%)	0 (0.0%)
	Chylorrhea	1 (1.7%)	1 (2.0%)	0 (0.0%)
	Paralytic ileus	1 (1.7%)	0 (0.0%)	1 (11.1%)

PC, partial colectomy; LHC, left hemicolectomy

Table 3: Postoperative recurrences in patients excluding pathological Stage IV (n=54)

Recurrences			surgical procedure
Recurrences		n (%)	PC, n=46	LHC, n=8
Any recurrences		6 (11.1%)	5 (10.9%)	1 (12.5%)
	Peritoneal dissemination	4 (7.5%)	3 (6.5%)	1 (12.5%)
	Liver	1 (1.9%)	1 (2.2%)	0 (0.0%)
	Ovary	1 (1.9%)	1 (2.2%)	0 (0.0%)
	Lymph node	0 (0.0%)	0 (0.0%)	0 (0.0%)

PC, partial colectomy; LHC, left hemicolectomy;

Table 4: Surgical procedures and extent of LND determined by preoperative 3D-CTA

Surgical procedure	Extent of LND	n=60
LHC	lt-MCA + AcMCA + LCA	3 (5.0%)
LHC	lt-MCA + LCA	6 (10.0%)
PC	lt-MCA + AcMCA	5 (8.3%)
	AcMCA + LCA	9 (15.0%)
	lt-MCA	10 (16.7%)
	AcMCA	14 (23.3%)
	LCA	13 (21.7%)

LND, lymph node dissection; LHC, left hemicolectomy; PC, partial colectomy; lt-MCA, left branch of middle colic artery; AcMCA, accessory middle colic artery; LCA, left colic artery

Table 5: Comparison of demographics, clinicopathological dates, and surgical outcomes in patients with PC versus LHC

^aMedian (IQR)

*Statistically significant

PC, partial colectomy; LHC, left hemicolectomy; BMI, body mass index; ASA, American Society of Anesthesiologists; UICC, Union for International Cancer Control

No competing interests reported.

Preoperative simulation using 3D-CT angiography in splenic flexure colon cancer: a retrospective observational study

Status:

Version 1

Abstract

Figures

Introduction

Methods

Patients

Preoperative simulation by 3D-CTA

Surgical procedure

Study design

Statistical Analysis

Results

Patient demographics, clinicopathological dates, and surgical outcomes

Preoperative simulation via 3D-CTA

Comparison of Outcomes in Patients with PC versus LHC

Discussion

Conclusions

Abbreviations

Declarations

References

Tables

Additional Declarations

Status:

Version 1